California native and exotic perennial grasses differ in

advertisement
California native and exotic perennial grasses differ in
their response to soil nitrogen, exotic annual grass
density, and order of emergence
The MIT Faculty has made this article openly available. Please share
how this access benefits you. Your story matters.
Citation
J. Abraham, J. Corbin, and C. D’Antonio, “California native and
exotic perennial grasses differ in their response to soil nitrogen,
exotic annual grass density, and order of emergence,” Plant
Ecology, vol. 201, Apr. 2009, pp. 445-456.
As Published
http://dx.doi.org/10.1007/s11258-008-9467-1
Publisher
Springer Netherlands
Version
Author's final manuscript
Accessed
Wed May 25 18:23:39 EDT 2016
Citable Link
http://hdl.handle.net/1721.1/49479
Terms of Use
Article is made available in accordance with the publisher's policy
and may be subject to US copyright law. Please refer to the
publisher's site for terms of use.
Detailed Terms
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
California native and exotic perennial grasses
differ in their response to soil nitrogen, exotic
annual grass density, and order of emergence
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
Joel K. Abraham1*, Jeffrey D. Corbin1,2, and Carla M. D’Antonio1,3
39
40
1
41
42
2
43
44
45
3
University of California, Berkeley, Department of Integrative Biology, Berkeley, CA
94720-3140, USA.
Present Address: Union College, Department of Biological Sciences, Schenectady,
NY 12308, USA.
Present Address: University of California, Santa Barbara, Ecology, Evolution &
Marine Biology, Santa Barbara, CA 93106, USA.
*Author for correspondence: (email: jabraham@berkeley.edu; phone: +1-510-643-5782)
1
46
Keywords
47
48
Exotic species, fertilization, germination, invasion, priority effects, seedling dynamics
49
Abstract
50
51
52
53
54
55
56
57
58
59
60
61
62
63
64
65
66
67
68
69
70
71
72
73
74
75
76
77
Early emergence of plant seedlings can offer strong competitive advantages over
later-germinating neighbors through the preemption of limiting resources. This
phenomenon may have contributed to the persistent dominance of European annual
grasses over native perennial grasses in California grasslands, since the former
species typically germinate earlier in the growing season than the latter and grow
rapidly after establishing. Recently, European perennial grasses have been spreading
into both non-native annual and native perennial coastal grass stands in California.
These exotic perennials appear to be less affected by the priority effects arising from
earlier germination by European annual grasses. In addition, these species
interactions in California grasslands may be mediated by increasing anthropogenic or
natural soil nitrogen inputs. We conducted a greenhouse experiment to test the effects
of order of emergence and annual grass seedling density on native and exotic
perennial grass seedling performance across different levels of nitrogen availability.
We manipulated the order of emergence and density of an exotic annual grass
(Bromus diandrus) grown with either Nassella pulchra (a native perennial grass),
Festuca rubra (native perennial) or Holcus lanatus (exotic perennial), with and
without added nitrogen. Earlier B. diandrus emergence and higher B. diandrus
density resulted in greater reduction in the aboveground productivity of the perennial
grasses. However, B. diandrus suppressed both native perennials to a greater extent
than it did H. lanatus. Nitrogen addition had no effect on the productivity of native
perennials, but greatly increased growth of the exotic perennial H. lanatus, grown
with B. diandrus. These results suggest that the order of emergence of exotic annual
versus native perennial grass seedlings could play an important role in the continued
dominance of exotic annual grasses in California. The expansion of the exotic
perennial grass H. lanatus in coastal California may be linked to its higher tolerance
of earlier-emerging annual grasses and its ability to access soil resources amidst high
densities of annual grasses.
78
79
80
81
82
83
2
84
Introduction
85
The order of emergence among competitors affects the growth, survival, and
86
fecundity of plants across a wide range of species, especially in situations with well-
87
defined growth windows and high densities of competitors (Miller et al. 1994; Verdù
88
and Traveset 2005). Early emergence in relation to competitors can allow for
89
preemption of available resources by the early emerging species, yielding
90
disproportionate advantages (Ross and Harper 1972). Once established, the early-
91
emerging species may maintain dominance even if it is a relatively poor competitor
92
during later life-stages.
93
Priority effects have been well documented in grasses (Harper 1961; Ross and
94
Harper 1972; Miller 1987; D’Antonio et al. 2001), and may be of particular
95
importance in maintaining the current structure of California grasslands. These
96
grasslands have experienced extensive invasion by exotic annual grasses and steep
97
declines in native perennial bunchgrasses over the last two centuries (Heady 1988;
98
D’Antonio et al. 2007). The continued success of exotic annual grasses suggests some
99
competitive advantage over native perennial grasses (Dyer and Rice 1997; Hamilton
100
et al. 1999; Corbin et al. 2007), although the two groups coexist in some coastal
101
prairie sites (Heady et al. 1988; Stromberg et al. 2001). Several studies have shown
102
that mature native perennial grasses can successfully compete with exotic annuals
103
(e.g. Peart 1989b; Seabloom et al. 2003; Corbin and D’Antonio 2004b; Lulow 2006),
104
but the natives may be sensitive to competition with annual plants at the seedling
105
stage particularly because exotic annual grasses tend to emerge at much higher
106
densities and earlier than native perennial grasses (Dyer and Rice 1997; Hamilton et
107
al. 1999; Humphrey and Schupp 2004; DiVittorio et al. 2007). Exotic annual grasses
108
germinate days after the first fall or winter rains while native perennial grasses are
109
typically slower to germinate (e.g. Reynolds et al. 2001). Subsequent aboveground
3
110
production of exotic annual grasses outpaces that of native perennial grasses,
111
potentially reducing light, water, and nutrients available for emerging perennial
112
seedlings (Jackson and Roy 1986; Dyer and Rice 1999). While some native
113
bunchgrass adults are thought to be long-lived (Hamilton et al. 1999), they can
114
eventually succumb to drought, burrowing animals or other mortality sources. If they
115
cannot successfully recruit due to seedling competition from exotic annual grasses,
116
then populations should eventually decline.
117
Efforts to reintroduce native perennial bunchgrasses have had limited success
118
when annuals are present at their typical high densities (Wilson and Gerry 1995; Dyer
119
and Rice 1999; Clausnitzer et al. 1999; Brown and Rice 2000). Management
120
strategies that negate priority effects and reduce the strength of annual grass
121
competition via reduced performance or density should improve the survival of
122
perennial grass seedlings and increase the success of restoration efforts (Corbin et al.
123
2004). For example, supplementing native seed supply (Seabloom et al. 2003),
124
killing annual grasses or their seeds (Stromberg and Kephart 1996; Moyes et al.
125
2005), or the planting of native perennial grasses as seedling plugs rather than seeds
126
(Dyer et al. 1996; Buisson et al. 2006) increases native grass establishment in
127
restoration sites, demonstrating the strong role exotic annual seedling density plays in
128
the suppression of native perennial grass establishment.
129
Beyond the competitive advantage gained by exotic annual grasses via earlier
130
and abundant germination, grassland restoration efforts in California also need to deal
131
with large increases in soil nitrogen availability due to atmospheric nitrogen
132
deposition and colonization by nitrogen-fixing shrubs (Maron and Connors 1996;
133
Vitousek et al. 1997; Weiss 1999, 2006; Fenn et al. 2003; Haubensak et al. 2004; Dise
134
and Stevens 2005). Increases in soil nitrogen availability are hypothesized to confer a
135
competitive advantage to fast-growing exotic species (Vitousek et al. 1987; Huenneke
4
136
et al. 1990; Burke and Grime 1996), and appear to disproportionately benefit exotic
137
annual grasses in California (e.g. Huenneke et al. 1990; Maron and Connors 1996;
138
Kolb et al. 2002; Lowe et al. 2003). For example, encroachment by non-native
139
annual grasses onto serpentine-derived soils, long a refuge from exotic annual grass
140
competition for many California native grassland species, occur when soil nitrogen
141
levels become elevated (Huenneke et al. 1990; Weiss 1999). Continued increases in
142
nitrogen deposition predicted through the next century (Phoenix et al. 2006; Weiss
143
2006) could have widespread consequences for patterns of exotic species invasion
144
and spread. Restoration strategies in California coastal grasslands will need to
145
include the direct and indirect effects of soil nitrogen enrichment on native perennial
146
grass versus exotic annual grass performance.
147
Even as restoration efforts to reestablish native perennial grasses continue,
148
exotic perennial grasses such as Holcus lanatus, Festuca arundinaceae, and Phalaris
149
aquatica have begun a second transformation of some areas in western grasslands
150
(Elliott and Wehausen 1974; Foin and Hektner 1986; Peart 1989a; Ewing 2002). The
151
ability of exotic perennial grasses to colonize the same annual-dominated stands that
152
have excluded native perennial reestablishment (Foin and Hektner 1986; Peart 1989c)
153
suggests that at least some European perennial grass species are less susceptible to
154
priority effects and competition from annual grasses. Given the shared life-history of
155
California and European perennial bunchgrasses, the differential success of exotic
156
versus native perennials may be linked to subtle differences in reproductive output,
157
germination timing or seedling growth traits, or responses to soil nitrogen enrichment.
158
For example, Holcus lanatus, a common exotic perennial invader in mesic coastal
159
grassland, produces copious seed (Peart 1989a), has higher relative growth rates than
160
some California native perennial grass species (Thomsen et al. 2006a; Corbin and
161
D’Antonio unpublished data), and appears to be highly responsive to nitrogen
5
162
enrichment (Schippers et al. 1999; Thomsen et al. 2006a). This species may thus be
163
less hindered than native perennial grasses by rapidly germinating exotic annuals or
164
high soil nitrogen availability at the seedling stage. Comparisons of the performance
165
of native vs. exotic perennial grass seedlings when faced with soil nitrogen
166
enrichment or competition with exotic annual grasses may help explain the disparity
167
in their ability to colonize annual dominated grasslands.
168
Our objective in this study was to determine the importance of annual grass
169
emergence time and density to the growth of native and exotic perennial grass
170
seedlings with and without nitrogen addition. We hypothesized that:
171
1) Reversing the typical “annual-followed-by-perennial grass” order of
172
emergence should increase perennial (native and exotic) grass seedling growth
173
by negating the priority effect.
174
2) Performance of the native perennial grass seedlings should be reduced to a
175
greater extent than performance of exotic perennial grass seedlings when
176
grown with high densities of exotic annual grasses.
177
3) The negative impact of exotic annual grasses on native perennial grasses
178
should be greater with added nitrogen because of the greater ability of annuals
179
to respond rapidly to increased resource availability. By contrast, N addition
180
should either have no effect or benefit exotic perennials grown with exotic
181
annuals.
182
We tested these hypotheses in a greenhouse using grass seedlings grown from
183
seed. We experimentally manipulated annual grass emergence time, annual grass
184
density, and soil nitrogen availability and tracked performance of native and non-
185
native perennial grasses.
186
6
187
Materials and Methods
188
Study Species and Source Population Description
189
We chose Nassella pulchra A. Hitchcock (Barkworth), Festuca rubra L., and Holcus
190
lanatus L. as the target perennial species, and Bromus diandrus Roth as the annual
191
competitor. Henceforward, the grasses will be referred to by their generic names; all
192
nomenclature follows Hickman (1993). These grass species co-occur in their ranges
193
in California (Hickman 1993). Nassella is a native perennial grass that was
194
historically abundant throughout California (Heady 1988), is among the most
195
common native bunchgrasses today in the California Floristic Province (Bartolome
196
and Gemmill 1981), and is a widely used species in grassland restoration. Festuca is
197
a coastally restricted species that remains abundant in some remnant prairies
198
(Stromberg et al. 2001). Holcus is an exotic perennial invader in mesic coastal and
199
inland California grasslands, encroaching on both non-native annual dominated and
200
remnant native perennial patches (Peart 1989a; Corbin et al. 2007). Bromus is a
201
widespread Eurasian species that appears to be a strong competitor in California
202
annual grasslands (Wilken and Painter 1993), particularly in more nitrogen-rich sites
203
(Maron and Jefferies 1999; Rice and Nagy 2000; Hoopes and Hall 2002).
204
We collected seeds of all of the species at Tom’s Point Preserve (38°13’N,
205
122°57’W), a private nature reserve near Tomales, CA, USA. The site has been the
206
location for a number of field studies focused on competition and resource use of
207
native perennial, exotic perennial, and exotic annual grasses (e.g. Corbin and
208
D’Antonio 2004a,b; Corbin et al. 2005; DiVittorio et al. 2007). The vegetation is a
209
mosaic of exotic annual, native perennial or exotic perennial species with large
210
patches of Holcus and Bromus.
211
7
212
Experimental Design
213
We conducted the experiment in the Oxford Tract Greenhouse at the University of
214
California, Berkeley from March 8, 2002 to June 4, 2002 under ambient temperature
215
conditions. We arranged the experiment in a randomized full factorial design, with
216
the following fixed factors: focal perennial species (Nassella, Festuca, Holcus),
217
Bromus density (low, high), nitrogen availability (low, high), and Bromus emergence
218
time (simultaneous, delayed). All pots were mixed species in that they had Bromus
219
with three individuals of one of the perennial grass species. In addition to the mixed
220
species pots, we planted perennial grasses in monoculture (three individuals) and
221
crossed the monoculture treatments with nitrogen availability to measure perennial
222
grass response without interspecific competitors. The monoculture pots with ambient
223
nitrogen treatment for each perennial species served as a baseline of growth for that
224
species (see below). We replicated each treatment eight times.
225
Using a 50% fine sand, 50% peat moss soil mix (UC mix) we planted seeds of
226
a given focal species (Nassella, Festuca or Holcus) in each perennial treatment pot
227
(10 L, 20 cm diameter). After emergence, we thinned the germinated plants in each
228
pot to three seedlings spaced a minimum of 5 cm from each other and the side of the
229
pot. We transplanted additional seedlings to pots with fewer than three emerged
230
perennials.
231
We planted Bromus seeds either concurrently with the planting of the
232
perennial seeds (“simultaneous”) or 14 days afterwards (“delayed”). This design
233
allowed us to evaluate how variation in early seedling growth timing interacts with
234
exotic annual density and identity of the competitor (perennial species).
235
We planted Bromus at two densities: “high” (1592 seeds m-2, 50 seeds/pot)
236
and “low” (637 seeds m-2, 20 seeds/pot). We based our high-density treatment on the
237
density of annual seeds found in an equivalent area of Bromus dominated stands at
8
238
Tom’s Point preserve (DiVittorio et al. unpublished data) and elsewhere in the state
239
(Young et al. 1981). The low-density treatment was meant to approximate annual
240
grass seed densities reduced by management, but is not based on field measurements.
241
To create the “high” soil nitrogen treatment, we added 0.93 g of blood meal
242
(Green All 100% Organic Blood Meal; 13-0-0) to the wet soil surface in three doses
243
(0, 30, 60 days after perennial planting). This “high” level of nitrogen addition (10 g
244
N m-2 over the course of the experiment) is consistent with estimates of soil nitrogen
245
input by nitrogen fixing shrubs in some coastal grasslands (Maron and Jefferies 1999;
246
Haubensak et al. 2004) and falls within the range of nitrogen fertilization used in
247
previous grassland studies (e.g. Inouye and Tilman 1988). No nitrogen was added to
248
the “low” soil nitrogen treatment.
249
We positioned pots randomly with respect to treatment in the greenhouse, and
250
rotated within and between benches every two weeks. We watered plants to soil
251
saturation three or four times per week. At the first appearance of a developing
252
Bromus flowering culm, we destructively sampled all plants by cutting at the soil
253
surface and separated material by species. After drying the aboveground plant
254
material in an oven at 70°C for two days, we recorded the mean individual dry
255
biomass of each species by pot.
256
257
Statistical Analysis
258
We converted biomass measurements into an index of relative shoot yield per plant
259
(RYP), calculated as the perennial biomass in an experimental treatment divided by
260
the mean biomass of the conspecific monoculture treatment plants in ambient
261
nitrogen (hereafter referred to as control): RYP = Biomassexperimental / Mean
262
Biomasscontrol. This index allowed us to compare across the perennial grasses in
9
263
evaluating the relative effect of the treatments on their growth (Johansson and Keddy
264
1991).
265
We performed all statistical tests with SYSTAT 11.0 (Systat Software, Inc.).
266
Our analysis began with a general assessment of the impact of Bromus on perennial
267
grass performance using a series of one-sample t-tests. We conducted one t-test for
268
each species to compare actual growth in competition with Bromus to growth in a
269
hypothetical null model (RYP = 1). Competitive treatments were pooled across
270
Bromus density, Bromus emergence time, and nitrogen addition. We then determined
271
the effect of nitrogen availability on perennial species growth in monoculture with a
272
two-factor ANOVA, using species identity and nitrogen availability as independent
273
fixed factors. We evaluated the independent and interactive effects of Bromus
274
density, emergence timing, nitrogen availability, and perennial species identity with a
275
separate four-factor analysis of variance (ANOVA). We used Tukey HSD post-hoc
276
tests (α = 0.05) to make any appropriate pair-wise comparisons in the four and two–
277
factor ANOVA tests.
278
The RYP data used in the t-tests were log transformed to improve normality
279
before analysis. Prior to application of the ANOVA tests we applied Cochran’s test
280
for unequal variances to the raw data to assess its heteroscedacity. The subset of
281
biomass data used in the two-way ANOVA passed Cochran’s test, so was left
282
untransformed. The RYP data used in the four-factor ANOVA failed Cochran’s test.
283
We again performed a log transformation to both normalize the data and reduce
284
heteroscedacity. The transformed RYP data did not pass the test, but was closer to
285
the given critical value. Because a balanced design ANOVA, such as that employed
286
in this study, is robust to minor departures from homogeneity of variances
287
(Underwood 1997; McGuinness 2002), we proceeded with the four-factor ANOVA
10
288
on the transformed data. We present back-transformed data and errors in figures
289
when data were transformed for analysis.
290
291
Results
292
Perennial response to Bromus presence
293
Growth of all three perennial species was suppressed in the presence of Bromus.
294
When compared to the hypothetical control RYP value of 1, the aboveground
295
production of Holcus (t = -9.983, df = 58, p < 0.0001), Nassella (t = -17.381, df = 63,
296
p < 0.0001), and Festuca (t = -23.150, df = 63, p < 0.0001) was significantly reduced
297
when grown with Bromus. However, the degree to which Bromus affected perennial
298
growth differed among species. Competitive treatments reduced Holcus growth by
299
nearly 75%. The two native perennials experienced even greater suppression:
300
Nassella growth was reduced by 85% while Festuca growth was reduced by 95%
301
(Figure 1).
302
303
Perennial response to nitrogen addition in monoculture
304
Nitrogen availability significantly interacted with perennial grass species identity in
305
the monoculture treatments (Table 1a). Holcus and Festuca, but not Nassella,
306
responded to nitrogen addition with increased aboveground growth (Figure 2).
307
Holcus grew significantly larger than the other two perennial species: in both the
308
ambient and added nitrogen treatments Holcus growth surpassed Festuca and
309
Nassella, while the aboveground production of the two native grasses was statistically
310
indistinguishable (Figure 2).
311
11
312
313
Perennial response to varying Bromus density, nitrogen addition, and
order of emergence
314
There were two significant three-way interactions in the four-factor ANOVA: 1)
315
Perennial sensitivity to Bromus density varied with nitrogen addition and order of
316
emergence, and 2) Perennial species identity interacted with Bromus density and
317
nitrogen addition (Table 1b). These interactions are discussed in detail below.
318
319
Bromus density x nitrogen addition x order of emergence
320
Delayed Bromus emergence significantly increased productivity of the perennial
321
grasses (Table 1b). Positive production responses by the perennials in delayed
322
Bromus emergence treatments occurred at both Bromus densities although the
323
‘release’ was stronger at low Bromus density (Figure 3). Nitrogen addition had no
324
effect on this pattern. High Bromus density generally resulted in lower perennial
325
grass growth, although the effect was negated in the simultaneous Bromus emergence
326
pots with added nitrogen (Figure 3).
327
12
328
Perennial species identity x Bromus density x nitrogen addition
329
The three perennials differed greatly in their responses to reduced Bromus density and
330
increased nitrogen availability (Table 1b). In the high nitrogen treatment, Holcus
331
RYP was significantly greater than that of Nassella or Festuca at both high and low
332
Bromus density (Figure 4). Nassella and Festuca, the two native species, responded
333
similarly to each other in the high nitrogen treatment.
334
nitrogen treatment Nassella outperformed Festuca and, at the high Bromus density,
335
outperformed Holcus. In the low Bromus density treatment, Holcus and Nassella
336
RYP were similar while Festuca RYP was significantly lower (Figure 4).
337
By contrast, in the low
Overall, Holcus experienced the least growth in the high Bromus density, low
338
nitrogen level treatment (Figure 4). Reduced Bromus density and increased soil
339
nitrogen availability tended to increase Holcus performance (Figure 4). Like Holcus,
340
Festuca exhibited the least growth in the high Bromus density treatment at the lower
341
nitrogen level. Although Festuca growth increased in the low Bromus density
342
treatment, overall, Festuca experienced the most consistent suppression by Bromus of
343
the three perennial grasses (Figure 4). In contrast to Holcus and Festuca, Nassella
344
experienced its lowest level of growth in high Bromus density with high soil nitrogen.
345
Nassella RYP was significantly increased with reductions in either nitrogen
346
availability or Bromus density.
347
348
Discussion
349
This study gauged the importance of density and timing of emergence of an abundant
350
annual grass on potentially coexisting perennial grasses under different levels of soil
351
fertility. The annual grass competitor Bromus suppressed growth of all three
352
perennial species relative to their growth in monoculture. As predicted, the level of
353
suppression tended to increase with Bromus density and decrease when perennial
13
354
grasses emerged before Bromus. Nitrogen addition increased the suppression of one
355
native perennial by Bromus, while the other native perennial showed no response.
356
Suppression of the exotic perennial by Bromus was decreased with nitrogen addition.
357
358
359
Order of emergence and density impacts on native perennial grass
seedling growth
360
Both the native and exotic perennial grasses responded strongly to delays in Bromus
361
emergence, increasing relative yield per plant (RYP) up to eight-fold (Figure 3). The
362
reduced Bromus density treatment similarly increased perennial grass RYP. The
363
strength of these responses demonstrates the potential importance of timing of
364
emergence for perennial grass seedlings and supports findings of previous studies in
365
California grasslands and other semi-arid grassland systems that highlight the
366
sensitivity of the seedling stage in perennial grasses (Bartolome and Gemmill 1981;
367
Dyer et al. 1996; Dyer and Rice 1997; Clausnitzer et al. 1999; Hamilton et al. 1999;
368
Brown and Rice 2000; Humphrey and Schupp 2004; Lenz and Facelli 2005).
369
California native perennial grasses must survive the summer drought, and accordingly
370
invest less in their aboveground growth or reproductive efforts in the first year than
371
do exotic annual grasses (Jackson and Roy 1986; Holmes and Rice 1996). Annual
372
grasses, on the other hand, must complete their life cycle before California’s annual
373
summer drought and so are among the earliest plants to germinate following the onset
374
of the rainy season. The high seedling densities and rapid aboveground growth
375
exhibited by exotic annual grasses creates an intense competitive environment for
376
later emerging seedlings (Jackson and Roy 1986; Corbin et al. 2007).
377
Priority effects have been reported in numerous systems across a broad range
378
of taxonomic groups (e.g. Harper 1961; Lawler and Morin 1993; Shorrocks and
379
Bingley 1994, D’Antonio et al. 2001; Kennedy and Bruns 2005). In California
14
380
grasslands, established native perennial stands are generally resistant to invasion by
381
exotic annual grasses (Seabloom et al. 2003; Corbin and D’Antonio 2004b; Lulow
382
2006), representing a priority effect manifested through arrival in a previous growing
383
season. However, priority effects for exotic annual grasses competing with perennial
384
seedlings occur over much shorter time scales. Previous work has shown that
385
differences in emergence timing of even a few days can be enough to reverse
386
competitive hierarchies between similar grass types (Harper 1961; Ross and Harper
387
1972; Rice and Dyer 2001). Some grasses, including Nassella, may even accelerate
388
emergence in response to annual grass neighbors, presumably to minimize the
389
impacts of later emergence (Dyer et al. 2000). Here we demonstrate the strong
390
priority effects that annual grasses can have on the seedlings of potentially coexisting
391
perennial grasses; reversing the order of emergence of the grass types had a large
392
effect on perennial grass seedling productivity, even when greatly outnumbered by an
393
exotic annual grass.
394
Early emergence and high densities of exotic annual seedlings are obstacles
395
that must be overcome for the restoration and maintenance of native-dominated
396
grasslands (Stromberg et al. 2007). Successful restoration of native perennial
397
grasslands often employs at least one of three strategies which improve perennial
398
seedling performance: increasing native seed input (e.g. Seabloom et al. 2003),
399
decreasing annual grass seed input/germination (e.g. Moyes et al. 2005), or planting
400
plugs of native perennial grasses rather than starting them from seed (e.g. Dyer et al.
401
1996; Huddleston and Young 2004). The first two strategies reduce the relative
402
abundance of exotic annual grasses, while the last, in effect, reverses the order of
403
emergence of exotic annual and native perennial grasses.
404
405
Once established, some stands of native perennials are able to exclude annual
grass invasion (Corbin and D’Antonio 2004b), and some studies suggest native
15
406
perennial grasses are stronger per-capita competitors than exotic annual grasses (e.g.
407
Seabloom et al. 2003; DiVittorio et al. 2007). However, the high rate of soil turnover
408
in California grasslands due to gopher and feral pig disturbance will create numerous
409
opportunities for exotic annual grasses to compete with native perennial seedlings
410
within restoration projects over the long-term (Hobbs and Mooney 1985, Kotanen
411
1995, Stromberg and Griffin 1996). Given that exotic annual propagule supply
412
grossly exceeds that of native perennials, asymmetry in competition through
413
emergence timing and density will likely limit the long-term ability of native
414
perennial grasses to reestablish dominance in restored areas unless disturbance is
415
minimized.
416
417
Nitrogen addition impacts on native perennial grass seedling growth
418
Differential responses to nitrogen addition between the two native perennial grass
419
species point toward differences in their ability to access this resource amidst
420
abundant exotic annual grass cover. Nassella in the monoculture treatment did not
421
increase aboveground growth following nitrogen addition, which suggests it was not
422
nitrogen limited in this study. Alternatively, the response could have been reflected
423
by reduced investment in belowground growth (Chapin 1980), which we did not
424
measure in this study. However, Nassella root:shoot did not decrease with nitrogen
425
fertilization in another study (Thomsen et al. 2006a). When nitrogen was added to
426
Nassella grown with a high density of Bromus, Nassella experienced a relative
427
decrease in aboveground growth. Festuca, on the other hand, did exhibit a positive
428
growth response to nitrogen addition in monoculture, demonstrating that it was
429
nitrogen limited. However, Festuca showed no response to nitrogen addition when
430
grown with Bromus, suggesting that Festuca was unable to benefit from added
431
nitrogen with neighboring annuals present. The responses of both Nassella and
16
432
Festuca are consistent with an indirect negative relationship between soil nitrogen
433
and native perennial grass performance due to increased productivity of exotic annual
434
grasses.
435
Our findings complement a number of studies in California and other semi-
436
arid grasslands that found that exotic annual grasses benefit disproportionately from
437
soil nitrogen supplementation relative to native perennial grasses (e.g. Huenneke et al.
438
1990; Maron and Conners 1996; Claassen and Marler 1998; Prober et al. 2002; Lowe
439
et al. 2003; Abraham et al. unpublished data; but see Kolb and Alpert 2003). This
440
suggests that native perennial grass seedlings are less likely to establish when faced
441
with both exotic annual grass competition and persistent or increasing soil nitrogen
442
enrichment. While this does not bode well for grassland restoration efforts, Seabloom
443
et al. (2003) found that, with seed supplementation, perennial grass seedlings were
444
capable of establishing in stands of exotic annual grasses across a gradient of nitrate
445
availability. However, their exotic annual grass stands were not dominated by
446
Bromus diandrus; it is possible that the identity of the annual grass competitor plays a
447
role in determining the outcome of perennial grass seedlings. D’Antonio and Corbin
448
(2004a) showed a first year reduction in annual grass suppression of native perennial
449
seedlings after soil amendment with sawdust (to reduce available soil nitrogen), but
450
found that there was no long-term benefit to the native grasses. Active management
451
of soil nitrogen levels may prove to be less important for maintenance of native
452
perennial dominated grasslands than reducing the density of exotic annual grass
453
competitors (DiVittorio et al. 2007).
454
455
Comparison of exotic and native perennial grass seedling response
456
Productivity, tolerance of annual grass competition, and response to resource pulses
457
differed significantly between native and exotic perennial grasses in this study. While
17
458
each perennial species responded to the inclusion of Bromus with marked reductions
459
in growth, Holcus tended to be less affected than either native perennial. Relative to
460
Festuca, Holcus suffered a smaller overall reduction in growth in every treatment
461
combination. In low nitrogen conditions, Nassella RYP was equal to or greater than
462
Holcus RYP. However, Nassella RYP was lower than that of Holcus when nitrogen
463
levels. Additionally, Holcus productivity was much greater than that of either native
464
perennial in monoculture (Figure 2).
465
A field study of Holcus establishment in exotic annual grasslands found that
466
Holcus seedling growth was not affected by competition with annual grasses
467
(Thomsen et al. 2006b). Thomsen et al. (2006a) also demonstrated that Holcus has
468
much higher initial relative growth rates than native perennial grasses, under both
469
high and low nitrogen conditions. Individual size in grasses is often positively
470
correlated with survival likelihood and competitive ability (Davies et al. 1999; Ewing
471
2002; Page and Bork 2005). As such, even if exotic annual grasses suppressed
472
Holcus, Festuca, and Nassella equally, Holcus would likely be better able to compete
473
with other grassland species due to its faster growth rate and larger size. Given the
474
results of this study and Thomsen et al. (2006b), it is likely that Holcus seedlings
475
better establish in exotic annual grass dominated stands than do native perennials.
476
Unlike the two native perennials, Holcus growth increased with additions of
477
nitrogen both in monoculture and in combination with Bromus, suggesting that
478
Holcus is a relatively strong competitor for soil resources with Bromus, at least when
479
water is not limiting as in this study. This response was mirrored in a field study;
480
elevated light and nutrient availability due to gopher disturbance increased Holcus
481
colonization relative to an exotic annual, Vulpia bromoides (Peart 1989c). Holcus
482
also showed increased productivity with higher nitrogen availability while in
483
competition with native perennial grasses (Schippers et al. 1999; Ewing 2002;
18
484
Thomsen et al. 2006a), so appears to be not only highly responsive to nitrogen
485
enrichment, but able to access that nitrogen alongside a range of potential
486
competitors.
487
488
Implications for management
489
California’s annual-dominated grasslands have excluded native perennial grasses for
490
decades, but in the coastal zone are often colonized by a number of exotic perennial
491
bunchgrass species; this suggests that there are critical differences between traits of
492
these native and exotic perennial grasses. In this study the native and exotic perennial
493
grasses we investigated responded differently to both soil fertilization and
494
competition with exotic annual grasses. Currently, common strategies for native
495
grass management are based on mitigating the emergence of exotic annual grasses,
496
and the associated negative effects of nitrogen enrichment that accompany their high
497
density and rapid growth. However, management tools to specifically limit the
498
encroachment of exotic perennial grass are largely undeveloped, and the efficacy of
499
current management techniques on limiting their spread is not well known (Stromberg
500
et al. 2007). Management practices that reduce annual grass seedling density could
501
inadvertently increase the abundance of Holcus, particularly in areas with high soil
502
nitrogen availability. As European perennial grasses become increasingly abundant
503
and widespread in California coastal grasslands, land management based on
504
generalizable life history differences among native perennial and exotic annual
505
grasses will lose efficacy. Successful management for native grassland species will
506
require continued research into the traits of a wider range of native and exotic
507
bunchgrasses and their species-specific responses to current restoration practices and
508
future environmental conditions.
19
509
Acknowledgements
510
511
512
513
514
515
516
517
We thank Barbara Rotz and the staff of the Oxford Tract Greenhouse for providing
space and support for this project. We also thank the Audubon Canyon Ranch for
allowing access to collect seed. A. D’Amore, M. Metz, J. Schue, N. Robinson, A.
Shabel, H. Schwartz, and E. Harris provided assistance in the greenhouse. W. Sousa,
M. Metz, K. Suttle, R. Bhaskar, J. Skene and two anonymous reviewers provided
useful comments on drafts of this manuscript. We thank the National Science
Foundation (DEB 9910008) for financial support.
518
References
519
520
521
522
523
524
525
526
527
528
529
530
531
532
533
534
535
536
537
538
539
540
541
542
543
544
545
546
547
548
549
550
551
552
553
554
Bartolome J W, Gemmill B (1981) The ecological status of Stipa pulchra (Poaceae)
in California. Madroño 28:172-184.
Brown C S, Rice K J (2000) The mark of Zorro: Effects of the exotic annual grass
Vulpia myuros on California native perennial grasses. Restor Ecol 8:10-17.
Buisson E, Holl K D, Anderson S, et al (2006) Effect of seed source, topsoil removal,
and plant neighbor removal on restoring California coastal prairies. Restor Ecol
14:569-577.
Burke M J W, Grime J P (1996) An experimental study of plant community
invasibility. Ecology 77:776-790.
Chapin F S (1980) The mineral nutrition of wild plants. Ann Rev Ecol Syst 11:233260.
Claassen V P, Marler M (1998) Annual and perennial grass growth on nitrogendepleted decomposed granite. Restor Ecol 6:175-180.
Clausnitzer D W, Borman M M, Johnson D E (1999) Competition between Elymus
elymoides and Taeniatherum caput-medusae. Weed Sci 47:720-728.
Corbin J D, D'Antonio C M (2004a) Can carbon addition increase competitiveness of
native grasses? A case study from California. Restor Ecol 12:36-43.
Corbin J D, D'Antonio C M (2004b) Competition between native perennial and exotic
annual grasses: Implications for an historical invasion. Ecology 85:1273-1283.
Corbin J D, D'Antonio C M, Bainbridge S (2004) Tipping the balance in the
restoration of native plants: Experimental approaches to changing the exotic:native
ratio in California grassland. In: Gordon M and Bartol S (eds), Experimental
approaches to conservation biology. University of California Press, Berkeley.
Corbin J D, Thomsen M A, Dawson T E, et al (2005) Summer water use by
California coastal prairie grasses: fog, drought, and community composition.
Oecologia 145:511-521.
20
555
556
557
558
559
560
561
562
563
564
565
566
567
568
569
570
571
572
573
574
575
576
577
578
579
580
581
582
583
584
585
586
587
588
589
590
591
592
593
594
595
596
597
598
599
600
601
602
603
604
605
Corbin J D, Dyer A R, Seabloom E W (2007) Competitive interactions. In: Stromberg
M R, Corbin J D and D'Antonio C M (eds), California grasslands: Ecology and
management. University of California Press, Berkeley.
D'Antonio C M, Hughes R F, Vitousek P M (2001) Factors influencing dynamics of
two invasive C-4 grasses in seasonally dry Hawaiian woodlands. Ecology 82:89-104.
D'Antonio C M, Malmstrom C, Reynolds S A, et al (2007) Ecology of invasive nonnative species in California grassland. In: Stromberg M R, Corbin J D and D'Antonio
C M (eds), California grasslands: Ecology and management. University of California
Press, Berkeley.
Davies A, Dunnett N P, Kendle T (1999) The importance of transplant size and gap
width in the botanical enrichment of species-poor grasslands in Britain. Restor Ecol
7:271-280.
Dise N B, Stevens C J (2005) Nitrogen deposition and reduction of terrestrial
biodiversity: Evidence from temperate grasslands. Sci China Ser C 48:720-728.
DiVittorio C T, Corbin J D, D'Antonio C M (2007) Spatial and temporal patterns of
seed dispersal: An important determinant of grassland invasion. Ecol Appl 17:311316.
Dyer A R, Fenech A, Rice K J (2000) Accelerated seedling emergence in interspecific
competitive neighbourhoods. Ecol Lett 3:523-529.
Dyer A R, Fossum H C, Menke J W (1996) Emergence and survival of Nassella
pulchra in a California grassland. Madroño 43:316-333.
Dyer A R, Rice K J (1997) Intraspecific and diffuse competition: The response of
Nassella pulchra in a California grassland. Ecol Appl 7:484-492.
Dyer A R, Rice K J (1999) Effects of competition on resource availability and growth
of a California bunchgrass. Ecology 80:2697-2710.
Elliott H W I, Wehausen J D (1974) Vegetation succession on coastal rangeland of
Point Reyes Peninsula. Madroño 22:231-238.
Ewing K (2002) Effects of initial site treatments on early growth and three-year
survival of Idaho fescue. Restor Ecol 10:282-288.
Fenn M E, Baron J S, Allen E B, et al (2003) Ecological effects of nitrogen deposition
in the western United States. Bioscience 53:404-420.
Foin T C, Hektner M M (1986) Secondary succession and the fate of native species in
a California coastal prairie community. Madroño 33:189-206.
Hamilton J G, Holzapfel C, Mahall B E (1999) Coexistence and interference between
a native perennial grass and non-native annual grasses in California. Oecologia
121:518-526.
21
606
607
608
609
610
611
612
613
614
615
616
617
618
619
620
621
622
623
624
625
626
627
628
629
630
631
632
633
634
635
636
637
638
639
640
641
642
643
644
645
646
647
648
649
650
651
652
653
654
655
Harper J L (1961) Approaches to the study of plant competition. Mechanisms in
Biological Competition. Academic Press Inc., New York.
Haubensak K A, D'Antonio C M, Alexander J (2004) Effects of nitrogen-fixing
shrubs in Washington and coastal California. Weed Technol 18:1475-1479.
Heady H F (1988) Valley grassland. In: Barbour M G and Major J (eds), Terrestrial
vegetation of California. California Native Plant Society, Sacramento.
Heady H F, Foin T C, Hektner M M, et al (1988) Coastal prairie and northern coastal
scrub. In: Barbour M G and Major J (eds), Terrestrial vegetation of California.
California Native Plant Society, Sacramento.
Hickman J C (ed) (1993) The Jepson Manual. University of California Press,
Berkeley, CA.
Hobbs R J, Mooney H A (1985) Community and population dynamics of serpentine
grassland annuals in relation to gopher disturbance. Oecologia 67:342-351.
Holmes T H, Rice K J (1996) Patterns of growth and soil-water utilization in some
exotic annuals and native perennial bunchgrasses of California. Ann Bot-London
78:233-243.
Hoopes M F, Hall L M (2002) Edaphic factors and competition affect pattern
formation and invasion in a California grassland. Ecol Appl 12:24-39.
Huddleston R T, Young T P (2004) Spacing and competition between planted grass
plugs and preexisting perennial grasses in a restoration site in Oregon. Restor Ecol
12:546-551.
Huenneke L F, Hamburg S P, Koide R, et al (1990) Effects of soil resources on plant
invasion and community structure in Californian serpentine grassland. Ecology
71:478-491.
Humphrey L D, Schupp E W (2004) Competition as a barrier to establishment of a
native perennial grass (Elymus elymoides) in alien annual grass (Bromus tectorum)
communities. J Arid Environ 58:405-422.
Inouye R S, Tilman D (1988) Convergence and divergence of old field plant
communities along experimental nitrogen gradients. Ecology 69:995-1004.
Jackson L E, Roy J (1986) Growth patterns of Mediterranean annual and perennial
grasses under simulated rainfall regimes of southern France and California. Acta
Oecol-Oec Plant 7:191-212.
Johansson M E, Keddy P A (1991) Intensity and asymmetry of competition between
plant pairs of different degrees of similarity: An experimental study on two guilds of
wetland plants. Oikos 60:27-34.
22
656
657
658
659
660
661
662
663
664
665
666
667
668
669
670
671
672
673
674
675
676
677
678
679
680
681
682
683
684
685
686
687
688
689
690
691
692
693
694
695
696
697
698
699
700
701
702
703
704
705
706
Kennedy P G, Bruns T D (2005) Priority effects determine the outcome of
ectomycorrhizal competition between two Rhizopogon species colonizing Pinus
muricata seedlings. New Phytol 166:631-638.
Kolb A, Alpert P (2003) Effects of nitrogen and salinity on growth and competition
between a native grass and an invasive congener. Biological Invasions 5:229-238.
Kolb A, Alpert P, Enters D, et al (2002) Patterns of invasion within a grassland
community. J Ecol 90:871-881.
Kotanen P M (1995) Responses of vegetation to a changing regime of disturbance effects of feral pigs in a Californian coastal prairie. Ecography 18:190-199.
Lawler S P, Morin P J (1993) Temporal Overlap, Competition, and Priority Effects in
Larval Anurans. Ecology 74:174-182.
Lenz T I, Facelli J M (2005) The role of seed limitation and resource availability in
the recruitment of native perennial grasses and exotics in a South Australian
grassland. Austral Ecol 30:684-694.
Lowe P N, Lauenroth W K, Burke I C (2003) Effects of nitrogen availability on
competition between Bromus tectorum and Bouteloua gracilis. Plant Ecol 167:247254.
Lulow M E (2006) Invasion by non-native annual grasses: The importance of species
biomass, composition, and time among California native grasses of the Central
Valley. Restor Ecol 14:616-626.
Maron J L, Connors P G (1996) A native nitrogen-fixing shrub facilitates weed
invasion. Oecologia 105:302-312.
Maron J L, Jefferies R L (1999) Bush lupine mortality, altered resource availability,
and alternative vegetation states. Ecology 80:443-454.
McGuinness K A (2002) Of rowing boats, ocean liners and tests of the ANOVA
homogeneity of variance assumption. Austral Ecol 27:681-688.
Miller T E (1987) Effects of emergence time on survival and growth in an early old
field plant community. Oecologia 72:272-278.
Miller T E, Winn A A, Schemske D W (1994) The effects of density and spatial
distribution on selection for emergence time in Prunella vulgaris (Lamiaceae). Am J
Bot 81:1-6.
Moyes A B, Witter M S, Gamon J A (2005) Restoration of native perennials in a
California annual grassland after prescribed spring burning and solarization. Restor
Ecol 13:659-666.
Page H N, Bork E W (2005) Effect of planting season, bunchgrass species, and
neighbor control on the success of transplants for grassland restoration. Restor Ecol
13:651-658.
23
707
708
709
710
711
712
713
714
715
716
717
718
719
720
721
722
723
724
725
726
727
728
729
730
731
732
733
734
735
736
737
738
739
740
741
742
743
744
745
746
747
748
749
750
751
752
753
754
755
756
757
Peart D R (1989a) Species interactions in a successional grassland .1. Seed rain and
seedling recruitment. J Ecol 77:236-251.
Peart D R (1989b) Species interactions in a successional grassland .2. Colonization of
vegetated sites. J Ecol 77:252-266.
Peart D R (1989c) Species interactions in a successional grassland .3. Effects of
canopy gaps, gopher mounds and grazing on colonization. J Ecol 77:267-289.
Phoenix G K, Hicks W K, Cinderby S, et al (2006) Atmospheric nitrogen deposition
in world biodiversity hotspots: the need for a greater global perspective in assessing N
deposition impacts. Global Change Biol 12:470-476.
Prober S M, Thiele K R, Lunt I D (2002) Identifying ecological barriers to restoration
in temperate grassy woodlands: soil changes associated with different degradation
states. Aust J Bot 50:699-712.
Reynolds S A, Corbin J D, D'Antonio C M (2001) The effects of litter and
temperature on the germination of native and exotic grasses in a coastal California
grassland. Madroño 48:230-235.
Rice K J, Nagy E S (2000) Oak canopy effects on the distribution patterns of two
annual grasses: The role of competition and soil nutrients. Am J Bot 87:1699-1706.
Ross M A, Harper J L (1972) Occupation of biological space during seedling
establishment. J Ecol 60:77-88.
Schippers P, Snoeijing I, Kropff M J (1999) Competition under high and low nutrient
levels among three grassland species occupying different positions in a successional
sequence. New Phytol 143:547-559.
Seabloom E W, Harpole W S, Reichman O J, et al (2003) Invasion, competitive
dominance, and resource use by exotic and native California grassland species. P Natl
Acad Sci USA 100:13384-13389.
Shorrocks B, Bingley M (1994) Priority effects and species coexistence - experiments
with fungal-breeding Drosophila. J Anim Ecol 63:799-806.
Stromberg M R, Griffin J R (1996) Long-term patterns in coastal California
grasslands in relation to cultivation, gophers, and grazing. Ecol Appl 6:1189-1211.
Stromberg M R, Kephart P (1996) Restoring native grasses in California old fields.
Restoration and Management Notes 14:102-111.
Stromberg M R, Kephart P, Yadon V (2001) Composition, invasibility, and diversity
in coastal California grasslands. Madroño 48:236-252.
Stromberg M R, D'Antonio C M, Young T P, et al (2007) California grassland
restoration. In: Stromberg M R, Corbin J D and D'Antonio C M (eds), California
grasslands: Ecology and management. University of California Press, Berkeley.
24
758
759
760
761
762
763
764
765
766
767
768
769
770
771
772
773
774
775
776
777
778
779
780
781
782
783
784
785
786
787
788
789
790
791
792
793
794
795
796
797
798
799
800
801
802
803
804
805
806
807
808
Thomsen M A, Corbin J D, D'Antonio C M (2006) The effect of soil nitrogen on
competition between native and exotic perennial grasses from northern coastal
California. Plant Ecol 186:23-35.
Thomsen M A, D'Antonio C M, Suttle K B, et al (2006) Ecological resistance, seed
density and their interactions determine patterns of invasion in a California coastal
grassland. Ecol Lett 9:160-170.
Underwood A J (1997) Experiments in ecology: their logical design and interpretation
using analysis of variance. Cambridge University Press, Cambridge.
Verdù M, Traveset A (2005) Early emergence enhances plant fitness: A
phylogenetically controlled meta-analysis. Ecology 86:1385-1394.
Vitousek P M, Aber J D, Howarth R W, et al (1997) Human alteration of the global
nitrogen cycle: Sources and consequences. Ecol Appl 7:737-750.
Vitousek P M, Walker L R, Whiteaker L D, et al (1987) Biological invasion by
Myrica faya alters ecosystem development in Hawaii. Science 238:802-804.
Weiss S B (1999) Cars, cows, and checkerspot butterflies: Nitrogen deposition and
management of nutrient-poor grasslands for a threatened species. Conserv Biol
13:1476-1486.
Weiss S B (2006) Impacts of nitrogen deposition on California ecosystems and
biodiversity. California Energy Commission, PIER Energy-Related Environmental
Research.
CEC-500-2005-165.
Wilken D H, Painter E L (1993) Bromus. In: Hickman J C (ed), The Jepson Manual.
University of California Press, Berkeley, CA.
Wilson S D, Gerry A K (1995) Strategies for mixed-grass prairie restoration:
Herbicide, tilling, and nitrogen manipulation. Restor Ecol 3:290-298.
Young J A, Evans R A, Larsen J R (1981) Germinable seeds and periodicity of
germination in annual grasslands. Hilgardia 49:1-35.
25
809
810
811
812
813
814
Table 1. Summary of two-factor and four-factor ANOVA tests. a) Two-factor
ANOVA. Effect of perennial species identity (PS) and nitrogen availability (N) on
aboveground production. b) Four-factor ANOVA. Effects of perennial species
identity (PS), Bromus emergence time (BET), Bromus density (BD), and nitrogen
availability (N) on relative shoot yield per plant. Significant results are in bold.
a) Two-Factor ANOVA
Treatment
df
Mean-Square
F
P
Perennial Species
2
47.808
161.19
<0.001
Nitrogen
1
6.695
22.573
<0.001
PS x N
2
1.841
6.209
0.004
Error
40
0.297
Treatment
df
Mean-Square
F
Perennial Species
2
45.797
32.823
<0.001
Bromus Emergence Time 1
296.475
212.490
<0.001
Bromus Density
1
26.100
18.707
<0.001
Nitrogen
1
7.133
5.113
0.025
PS x BET
2
4.573
3.278
0.040
PS x BD
2
0.160
0.115
0.892
PS x N
2
15.665
11.228
<0.001
BET x N
1
0.211
0.151
0.698
BET x BD
1
0.841
0.603
0.439
BD x N
1
5.412
3.879
0.051
PS x BET x BD
2
0.467
0.335
0.716
PS x BET x N
2
3.722
2.668
0.072
PS x BD x N
2
5.012
3.592
0.030
BET x BD x N
1
7.240
5.189
0.024
PS x BET x BD x N
2
1.463
1.049
0.353
162
1.395
b) Four-Factor ANOVA
Error
P
815
816
817
818
819
820
26
821
822
823
824
Figure 1. Relative shoot yield of perennials (RYP) in response to competition with
Bromus, averaged across all Bromus density, nitrogen, and Bromus emergence time
treatments (mean ± 1 SE). An RYP below 1 suggests a reduction in growth with
Bromus competitors relative to growth in monoculture.
825
826
827
828
829
Figure 2. Perennial aboveground growth in monoculture with and without nitrogen
addition (mean ± 1 SE). Vertical lines indicate non-significant differences within a
given nitrogen treatment. Asterisks indicate differences within a single species across
nitrogen treatments; ‘n.s.’ indicates non-significance.
830
831
832
833
834
835
836
Figure 3. Relative shoot yield of perennials (RYP) in high and low Bromus density
treatments at simultaneous and late Bromus emergence times, separated by nitrogen
addition treatment (mean ± 1 SE). Horizontal lines indicate non-significant
differences within a given nitrogen and emergence time treatment combination.
Shared letters indicate non-significant differences within a given density of Bromus
across nitrogen addition and emergence time treatment combinations.
837
838
839
840
841
842
843
844
845
846
847
848
849
850
851
852
853
854
855
856
857
858
859
860
861
862
863
864
865
866
867
868
Figure 4. Relative shoot yield of perennials (RYP) with and without nitrogen
addition, separated by Bromus density treatment (mean ± 1 SE). Horizontal lines
indicate non-significant differences within a given density and nitrogen treatment
combination. Shared letters indicate non-significant differences within a single
species across all density and nitrogen treatment combinations.
*
*
27
869
870
871
Figure 1
872
873
874
875
876
877
878
879
880
881
882
883
884
885
886
887
888
889
890
891
892
893
894
895
896
897
898
28
899
Figure 2
900
901
902
903
904
905
906
907
908
909
910
29
911
Figure 3
912
913
914
915
916
917
918
919
920
921
922
30
923
Figure 4
924
925
926
927
31
Download